Comparative analysis of natural vs artificial Mn₄Ca clusters: Structural insights into O-O bond formation in photosystem II

The oxygen-evolving center (OEC) of photosystem II (PSII) is a unique Mn4CaO5 cluster that catalyzes the water-splitting reaction to produce electrons, protons, and dioxygen. Recently, the detailed structures of the OEC in different S-states have been revealed by X-ray free-electron laser (XFEL). To facilitate understanding the structure-function relationship of the OEC, a series of artificial Mn4CaO4 clusters have been synthesized, which closely mimic the main metal-oxide core and peripheral ligands, as well as the redox properties of the OEC. Herein, we have systematically analyzed the oxidation states of all Mn ions in the structural data of the OEC revealed by XFEL and artificial Mn4CaO4 clusters. It shows that the oxidation states of some Mn ions in structural data of OEC are significantly lower than the expected values in native PSII, suggesting the occurrence of the reduction of high-valent Mn ions induced by XFEL, whereas all Mn ions in artificial Mn4CaO4 clusters have the same oxidation states as those in the S1 state OEC in native PSII. Furthermore, for the first time, we have observed that the missing μ2-O bridge in the artificial Mn4CaO4 cluster can be generated in solution, forming an unstable Mn4CaO5 cluster, which supports that this μ2-O bridge (O4) is exchangeable and may serve as the active site for O-O bond formation in the cluster. These results provide new insights into the catalytic mechanism of the oxygen-evolving reaction in both natural and artificial photosynthesis.